eMedicine Specialties > Infectious Diseases > Bacterial Infections

Enterobacter Infections

Author: Susan L Fraser, MD, Infectious Diseases Service, Walter Reed Army Medical Center; Chairman, Infection Control Committee; Associate Professor of Medicine, Uniformed Services University of the Health Sciences
Coauthor(s): Michael Arnett, MD, Resident, Department of Medicine, Tripler Army Medical Center; Christian P Sinave, MD, Associate Professor, Department of Medical Microbiology and Infectious Diseases, University of Sherbrooke, Canada
Contributor Information and Disclosures

Updated: Aug 28, 2008

Introduction

Background

Enterobacter species, particularly Enterobacter cloacae and Enterobacter aerogenes, are important nosocomial pathogens responsible for various infections, including bacteremia, lower respiratory tract infections, skin and soft-tissue infections, urinary tract infections (UTIs), endocarditis, intra-abdominal infections, septic arthritis, osteomyelitis, and ophthalmic infections. Enterobacter species can also cause various community-acquired infections, including UTIs, skin and soft-tissue infections, and wound infections, among others.

Risk factors for nosocomial Enterobacter infections include hospitalization of greater than 2 weeks, invasive procedures in the past 72 hours, treatment with antibiotics in the past 30 days, and the presence of a central venous catheter. Specific risk factors for infection with nosocomial multidrug-resistant strains of Enterobacter species include the recent use of broad-spectrum cephalosporins or aminoglycosides and ICU care.

These "ICU bugs" cause significant morbidity and mortality, and infection management is complicated by resistance to multiple antibiotics. Enterobacter species possess inducible beta-lactamases, which are undetectable in vitro but are responsible for resistance during treatment. Physicians treating patients with Enterobacter infections are advised to avoid certain antibiotics, particularly third-generation cephalosporins, because resistant mutants can quickly appear. The crucial first step is appropriate identification of the bacteria. Antibiograms must be interpreted with respect to the different resistance mechanisms and their respective frequency, as is reported for Enterobacter species, even if routine in vitro antibiotic susceptibility testing has not identified resistance.

Pathophysiology

Enterobacter species rarely cause disease in healthy individuals. This opportunistic pathogen, similar to other members of the Enterobacteriaceae family, possesses an endotoxin known to play a major role in the pathophysiology of sepsis and its complications.

Although community-acquired Enterobacter infections are occasionally reported, nosocomial Enterobacter infections are, by far, most common. Patients most susceptible to Enterobacter infections are those who stay in the hospital, especially the ICU, for prolonged periods. Other major risk factors of Enterobacter infection include prior use of antimicrobial agents, concomitant malignancy (especially hemopoietic and solid-organ malignancies), hepatobiliary disease, ulcers of the upper gastrointestinal tract, use of foreign devices such as intravenous catheters, and serious underlying conditions such as burns, mechanical ventilation, and immunosuppression.

The source of infection may be endogenous (via colonization of the skin, gastrointestinal tract, or urinary tract) or exogenous, resulting from the ubiquitous nature of Enterobacter species. Multiple reports have incriminated the hands of personnel, endoscopes, blood products, devices for monitoring intra-arterial pressure, and stethoscopes as sources of infection. Outbreaks have been traced to various common sources: total parenteral nutrition solutions, isotonic saline solutions, albumin, digital thermometers, and dialysis equipment.

Enterobacter species contain a subpopulation of organisms that produce a beta-lactamase at low-levels. Once exposed to broad-spectrum cephalosporins, the subpopulation of beta-lactamase–producing organisms predominate. Thus, an Enterobacter infection that appears sensitive to cephalosporins at diagnosis may quickly develop into a resistant infection during therapy. Carbapenems and cefepime have a more stable beta-lactam ring against the lactamase produced by resistant strains of Enterobacter.

Frequency

United States

National surveillance programs continually demonstrate that Enterobacter species remain a significant source of morbidity and mortality in hospitalized patients.

In the Surveillance and Control of Pathogens of Epidemiological Importance [SCOPE] project, 24,179 nosocomial bloodstream infections from 1995-2002 were analyzed. Enterobacter species were the second-most-common gram-negative organism behind Pseudomonas aeruginosa; however, both bacteria were reported to each represent 4.7% of bloodstream infections in ICU settings. Enterobacter species represent 3.1% of bloodstream infections in non-ICU wards. In a more recent report, of nearly 75,000 gram-negative organisms collected from ICU patients in the United States between 1993 and 2004, Enterobacter species comprised 13.5% of the isolates. Multidrug resistance increased over time, especially in infections caused by E cloacae.1

Previous reports from the National Nosocomial Infections Surveillance System (NNIS) demonstrated that Enterobacter species caused 11.2% of pneumonia cases in all types of ICUs, ranking third after Staphylococcus aureus (18.1%) and P aeruginosa (17%). The corresponding rates among patients in pediatric ICUs were 9.8% for pneumonia, 6.8% for bloodstream infections, and 9.5% for UTIs.2,3,4

Enterobacter species were also among the most frequent pathogens involved in surgical-site infections, as reported in the NNIS report from October 1986 to April 1997. The isolation rate was 9.5% (with enterococci, coagulase-negative staphylococci, S aureus, and P aeruginosa rates being 15.3%, 12.6%, 11.2%, and 10.3%, respectively).

Data on antibiotic resistance are available from the Intensive Care Antimicrobial Resistance Epidemiology (ICARE) surveillance report. The rates of Enterobacter resistance to third-generation cephalosporins were 25.3% in ICUs, 22.3% among non-ICU inpatients, 10.1% among ambulatory patients, and as high as 36.2% in pediatric ICUs.5

International

Enterobacter species have a global presence in both adult and neonatal ICUs. Surveillance data and outbreak case reports from North and South America, Europe, and Asia indicate that these bacteria represent an important opportunistic pathogen among neonates and debilitated patients in ICUs.

The prevalence of Enterobacter resistance to beta-lactam antibiotics, aminoglycosides, trimethoprim-sulfamethoxazole (TMP-SMZ), and quinolones seems to be higher in certain European countries and Israel than in the United States and Canada. Higher rates of Enterobacter resistance to fluoroquinolones and to beta-lactam and cephalosporin antibiotics due to the production of extended-spectrum beta-lactamases have been reported in South America and the Asian and Pacific regions.6,7

Mortality/Morbidity

Enterobacter infections cause considerable mortality and morbidity rates.

  • Enterobacter species can cause disease in virtually any body compartment. They are responsible for frequent and severe nosocomial infections that require prolonged hospitalization, multiple and varied imaging studies and laboratory tests, various surgical and nonsurgical procedures, and powerful and expensive antimicrobial agents. Most importantly, Enterobacter infections that do not directly causing death cause considerable suffering in many patients, most of whom are already afflicted with chronic diseases.
  • In patients with Enterobacter bacteremia, the most important factor in determining the risk of mortality is the severity of the underlying disease. Higher 30-day mortality rates were noted in patients presenting with septic shock and increasing Acute Physiology and Chronic Health Evaluation II scores. Other factors implicated, independently or by association, in the outcome of Enterobacter bacteremia include thrombocytopenia, hemorrhage, a concurrent pulmonary focus of infection, renal insufficiency, admission in an ICU, prolonged hospitalization, prior surgery, intravascular and/or urinary catheters, immunosuppressive therapy, neutropenia, antibiotic resistance, and inappropriate antimicrobial therapy.
  • Recent studies have demonstrated that empirical aminoglycoside use and appropriate initial antibiotic therapy were associated with lower mortality rates, whereas vasopressor use, ICU care, and acute renal failure were associated with higher mortality rates. Independent risk factors for mortality included cephalosporin resistance, trimethoprim-sulfamethoxazole resistance, mechanical ventilation, and nosocomial infection.8,9
  • Crude mortality rates associated with Enterobacter infections range from 15-87%, but most reported rates range from 20-46%. Attributable mortality rates are reported to range from 6-40%.
    • E cloacae infection is associated with the highest mortality rate of all Enterobacter infections.
    • Bacteremia with cephalosporin-resistant Enterobacter species is associated with a 30-day mortality rate that significantly exceeds that of infections with susceptible strains (33.7% vs 18.6%).
    • Mortality rates associated with Enterobacter pneumonia are higher than those of pneumonia due to many other gram-negative bacilli. These rates range from 14-71%. As with bacteremia, the severity of the underlying disease is the major factor that predicts outcome. Other factors that indicate an unfavorable outcome include the extent of the disease as seen on chest radiographs, corticosteroid therapy, isolation of multiple pathogens from lower respiratory tract secretions, and, possibly, treatment with a single antibiotic.
    • A review of 17 cases of Enterobacter endocarditis reported an overall mortality rate of 44.4%.

Race

  • Enterobacter infections have no reported or presumed racial predilection.

Sex

  • The male-to-female ratio of Enterobacter bacteremia is 1.3-2.5:1. This male predominance is also reported in the pediatric population.

Age

  • Enterobacter infections are most common in neonates and in elderly individuals, reflecting the increased prevalence of severe underlying diseases at these age extremes. In the pediatric ICU setting, an age younger than 2.5 years is a risk factor for colonization.
  • Enterobacter sakazakii has been reported as a cause of sepsis and meningitis, complicated by ventriculitis, brain abscess, cerebral infarction, and cyst formation.10 This clinical pattern appears to be specific to E sakazakii in neonates and infants infected with this bacterium. E sakazakii has also been associated with many outbreaks due to contaminated powdered formula for infants.11

Clinical

History

Enterobacter infections do not produce a unique enough clinical presentation to differentiate them clinically from other acute bacterial infections. Consequently, details on the patient history and physical examination findings for each infected body compartment are not provided in this article, with the exception of lower respiratory tract infections and bacteremia. Details regarding similar disease presentations are available throughout the eMedicine journal via the links provided in Differentials.

  • Bacteremia
    • Most cases of Enterobacter bacteremia are nosocomial, frequently acquired in the ICU.
    • E cloacae, followed by E aerogenes, are by far the species implicated most frequently in Enterobacter bacteremia cases.
    • Mixed bacteremia is common (14-53%).
    • The portal of entry into the bloodstream is frequently unknown, but any infected organ may be the primary source of bacteremia.
    • Symptoms of Enterobacter bacteremia are similar to those of bacteremia due to other gram-negative bacilli.
  • Lower respiratory tract infections
    • The clinical presentations caused by Enterobacter lower respiratory tract infections include asymptomatic colonization, tracheobronchitis, pneumonia, lung abscess, and empyema.
    • As with other respiratory pathogens, chronic obstructive pulmonary disease, diabetes mellitus, alcohol abuse, malignancy, and neurologic diseases are risk factors for the acquisition of lower respiratory tract infections.
    • Prior antimicrobial therapy may predispose to Enterobacter pneumonia.
    • Enterobacter species are a significant cause of ventilator-associated pneumonia.
    • Enterobacter species are major pathogens in early post–lung transplant pneumonia. In most cases, the bacteria are transmitted from the donor.
    • Symptoms of Enterobacter pneumonia are not specific to these bacteria. Fever, cough, production of purulent sputum, tachypnea, and tachycardia are usually present.
    • As with infections caused by organisms such as Streptococcus pneumoniae, many Enterobacter infections in elderly debilitated patients do not cause a systemic inflammatory reaction. However, this clinical presentation is by no means benign, and the associated mortality rate is particularly high in this population.
  • Skin and soft-tissue infections
    • In most cases, Enterobacter skin and soft-tissue infections are hospital-acquired and include cellulitis, fasciitis, myositis, abscesses, and wound infections.
    • Enterobacter species can infect surgical wounds in any body site, and these infections are clinically indistinguishable from infections caused by other bacteria.
    • In 1985, Palmer et al reviewed an outbreak of postsurgical Enterobacter mediastinitis.12 Cases varied in severity from fulminant bacteremic infections to less-severe wound infections. The source was unknown, and a case-control analysis suggested that surgical complications and prophylaxis with cephalosporins were associated with the infection. The level of skin and wound colonization was high among patients who underwent cardiac surgery during this outbreak. The outbreak was controlled with barrier isolation, restriction of contacts, and a reduction in the duration of cephalosporin prophylaxis.
    • Other Enterobacter wound infections have been reported in the literature. Infected body sites have included a posterior spinal wound, burn wounds (many reports), and different types of injuries involving trauma to multiple sites. Some of the infections were polymicrobial. Some authors have noted a trend of traditional wound bacteria (eg, S aureus) being replaced by Enterobacter species and other nosocomial pathogens. Some trauma-related wound infections are acquired before hospital admission. This was the case with agricultural mutilating wounds caused by corn-harvesting machines. Gram-negative rods were predominant (81%), the most common being Enterobacter species and Stenotrophomonas maltophilia.
    • Enterobacter species occasionally cause community-acquired soft-tissue infections in healthy individuals, including those who sustain war-related injuries.
  • Endocarditis
    • A case report described a patient with E cloacae endocarditis on a porcine mitral heterograft. An accompanying literature review disclosed 17 additional cases. Two thirds of the patients had underlying cardiac disease; most had mitral valve infection, and 4 patients had concomitant aortic valve involvement.13
    • A few more case reports subsequent to this case series have been published in both English and non-English literature.
  • Urinary tract infections
    • Enterobacter UTI is indistinguishable from a UTI caused by other gram-negative bacilli.
    • Pyelonephritis with or without bacteremia, prostatitis, cystitis, and asymptomatic bacteriuria can be caused by Enterobacter species, as with Escherichia coli and other gram-negative bacilli.
    • Most Enterobacter UTIs are nosocomial and are associated with indwelling urinary catheters and/or prior antibiotic therapy.
  • Intra-abdominal infections
    • Enterobacter species may be isolated together with colonic flora in intra-abdominal abscesses or peritonitis following intestinal perforation or surgery.
    • A frequent cause of Enterobacter involvement is prior digestive-tract colonization by Enterobacter species during hospitalization.
    • Case reports have described Enterobacter hepatobiliary sepsis, including emphysematous cholecystitis, suppurative cholangitis, and hepatic gas gangrene in a child after liver transplantation. Hemorrhagic necrotizing pancreatitis developed in a 72-year-old woman with obstructive jaundice.
  • Central nervous system infections
    • Neonatal meningitis resulting from E sakazakii infection is described in Age.
    • In 1993, Durand et al published a review of 493 episodes of acute bacterial meningitis.14 This study involved patients aged 16 years or older admitted to Massachusetts General Hospital from January 1962 through December 1988. Gram-negative bacilli were the etiologic agents in 4% and 38% of community-acquired and nosocomial meningitis, respectively. In community-acquired infections, Enterobacter was isolated in one of the 9 cases of meningitis caused by gram-negative bacilli (E coli 4 times, Klebsiella species 3 times, and Proteus once) and in 5 of the 57 episodes of nosocomial meningitis (E coli 17 times, Klebsiella species 13 times, Pseudomonas species 6 times, and Acinetobacter species 6 times).
    • Other series were reported from various countries (United States, Iceland, United Kingdom, Senegal, Brazil). Gram-negative bacilli were not among the 5 most common causes of meningitis in any of these countries.
  • Ophthalmic infections
    • Enterobacter species account for a small fraction of postsurgical endophthalmitis cases.
    • Most ophthalmic infections are caused by gram-positive organisms, but Enterobacter species and Pseudomonas species are among the most aggressive pathogens.
  • Bone and joint infections
    • Enterobacter species are occasionally implicated in septic arthritis, on both native and prosthetic joints, and can result in osteomyelitis and discitis in adults and children.
    • Enterobacter bone and joint infections are usually more difficult to cure than those caused by S aureus. The authors have observed relapses that required additional treatment following the initial 6 weeks of intravenous therapy.

Physical

  • Bacteremia
    • Physical examination findings consistent with systemic inflammatory response syndrome (SIRS) include heart rate that exceeds 90 bpm, a respiratory rate of greater than 20, and temperature of greater than 38°C or less than 36°C.
    • More than 80% of children and adults with Enterobacter bacteremia develop fever.
    • Hypotension and shock occur in as many as one third of cases.
    • Disseminated intravascular coagulation, jaundice, acute respiratory distress syndrome, and other organ failures reflect the severity of septic shock.
    • Purpura fulminans and hemorrhagic bullae usually observed with meningococci or viruses causing hemorrhagic fever may be part of the clinical presentation of Enterobacter bacteremia.
    • Ecthyma gangrenosum, usually associated with Pseudomonas or Aeromonas bacteremia, may also be observed.
    • Cyanosis and mottling is frequently reported in children with Enterobacter bacteremia.
  • Lower respiratory tract infections
    • The physical manifestations caused by Enterobacter are not specific for infection with these bacteria. Enterobacter lower respiratory tract infections can manifest identically to those caused by S pneumoniae or other organisms.
    • The physical examination findings may include apprehension, high fever or hypothermia, tachycardia, hypoxemia, tachypnea, and cyanosis. Patients with pulmonary consolidation may present with crackling sounds, dullness to percussion, tubular breath sounds, and egophony. Pleural effusion may manifest as dullness to percussion and decreased breath sounds.

Causes

  • Enterobacter is a gram-negative bacillus that belongs to the Enterobacteriaceae family. Other members of this family include Klebsiella, Escherichia, Citrobacter, Serratia, Salmonella, and Shigella species, among many others. Enterobacteriaceae are the most common bacterial isolates recovered from clinical specimens. These bacteria have an outer membrane that contains, among other things, lipopolysaccharides from which lipid-A plays a major role in sepsis. Lipid-A, also known as endotoxin, is the major stimulus for the release of cytokines, which are the mediators of systemic inflammation and its complications.
  • In the microbiology laboratory, colonies of Enterobacteriaceae appear large, dull-gray, and dry or mucoid on sheep blood agar. All Enterobacteriaceae ferment glucose and, consequently, are able to grow in aerobic and anaerobic atmospheres.
  • MacConkey agar is a lactose-containing medium that is selective for nonfastidious gram-negative bacilli such as Enterobacteriaceae. Using the enzymes beta-galactosidase and beta-galactoside permeases, the most frequently encountered species of Enterobacter strains activate the pH indicator (neutral red) included in MacConkey agar, giving a red stain to the growing colonies. Klebsiella and Enterobacter species may appear similar as mucoid colonies but can be differentiated with a few specific tests. In contrast to Klebsiella species, Enterobacter organisms are motile, usually ornithine decarboxylase-positive, and urease-negative.
  • Many different species comprise the genus Enterobacter. Some have never been associated with human infections. The most commonly isolated species include E cloacae and E aerogenes, followed by E sakazakii, which produces a characteristic yellow pigment. Other species rarely encountered in the clinic include Enterobacter asburiae, Enterobacter gergoviae, Enterobacter taylorae, Enterobacter hormaechei, and Enterobacter cancerogenus. Enterobacter agglomerans has been removed from the genus Enterobacter and renamed Pantoea agglomerans.

More on Enterobacter Infections

Overview: Enterobacter Infections
Differential Diagnoses & Workup: Enterobacter Infections
Treatment & Medication: Enterobacter Infections
Follow-up: Enterobacter Infections
Multimedia: Enterobacter Infections
References
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References

  1. Lockhart SR, Abramson MA, Beekmann SE, et al. Antimicrobial resistance among Gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol. Oct 2007;45(10):3352-9. [Medline].

  2. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) report, data summary from October 1986-April 1997, issued May 1997. A report from the NNIS System. Am J Infect Control. Dec 1997;25(6):477-87. [Medline].

  3. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) System report, data summary from January 1990-May 1999, issued June 1999. Am J Infect Control. Dec 1999;27(6):520-32. [Medline].

  4. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control. Dec 2004;32(8):470-85. [Medline].

  5. National Nosocomial Infections Surveillance System. Intensive Care Antimicrobial Resistance Epidemiology (ICARE) Surveillance Report, data summary from January 1996 through December 1997: A report from the National Nosocomial Infections Surveillance (NNIS) System. Am J Infect Control. Jun 1999;27(3):279-84. [Medline].

  6. Rossi F, Baquero F, Hsueh PR, et al. In vitro susceptibilities of aerobic and facultatively anaerobic Gram-negative bacilli isolated from patients with intra-abdominal infections worldwide: 2004 results from SMART (Study for Monitoring Antimicrobial Resistance Trends). J Antimicrob Chemother. Jul 2006;58(1):205-10. [Medline].

  7. Chow JW, Satishchandran V, Snyder TA, et al. In vitro susceptibilities of aerobic and facultative gram-negative bacilli isolated from patients with intra-abdominal infections worldwide: the 2002 Study for Monitoring Antimicrobial Resistance Trends (SMART). Surg Infect (Larchmt). Winter 2005;6(4):439-48. [Medline].

  8. Deal EN, Micek ST, Ritchie DJ, et al. Predictors of in-hospital mortality for bloodstream infections caused by Enterobacter species or Citrobacter freundii. Pharmacotherapy. Feb 2007;27(2):191-9. [Medline].

  9. Ye Y, Li JB, Ye DQ, et al. Enterobacter bacteremia: Clinical features, risk factors for multiresistance and mortality in a Chinese University Hospital. Infection. Oct 2006;34(5):252-7. [Medline].

  10. Gallagher PG, Ball WS. Cerebral infarctions due to CNS infection with Enterobacter sakazakii. Pediatr Radiol. 1991;21(2):135-6. [Medline].

  11. Drudy D, Mullane NR, Quinn T, et al. Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin Infect Dis. Apr 1 2006;42(7):996-1002. [Medline].

  12. Palmer DL, Kuritsky JN, Lapham SC, et al. Enterobacter mediastinitis following cardiac surgery. Infect Control. Mar 1985;6(3):115-9. [Medline].

  13. Tunkel AR, Fisch MJ, Schlein A, et al. Enterobacter endocarditis. Scand J Infect Dis. 1992;24(2):233-40. [Medline].

  14. Durand ML, Calderwood SB, Weber DJ, et al. Acute bacterial meningitis in adults. A review of 493 episodes. N Engl J Med. Jan 7 1993;328(1):21-8. [Medline].

  15. Maki DG, Weise CE, Sarafin HW. A semiquantitative culture method for identifying intravenous-catheter-related infection. N Engl J Med. Jun 9 1977;296(23):1305-9. [Medline].

  16. Paterson DL. Resistance in gram-negative bacteria: enterobacteriaceae. Am J Med. Jun 2006;119(6 Suppl 1):S20-8; discussion S62-70. [Medline].

  17. Ratnam I, Franklin C, Spelman DW. In vitro activities of 'new' and 'conventional' antibiotics against multi-drug resistant Gram negative bacteria from patients in the intensive care unit. Pathology. Dec 2007;39(6):586-8. [Medline].

  18. Reinert RR, Low DE, Rossi F, et al. Antimicrobial susceptibility among organisms from the Asia/Pacific Rim, Europe and Latin and North America collected as part of TEST and the in vitro activity of tigecycline. J Antimicrob Chemother. Nov 2007;60(5):1018-29. [Medline].

  19. Halstead DC, Abid J, Dowzicky MJ. Antimicrobial susceptibility among Acinetobacter calcoaceticus-baumannii complex and Enterobacteriaceae collected as part of the Tigecycline Evaluation and Surveillance Trial. J Infect. Jul 2007;55(1):49-57. [Medline].

  20. DiPersio JR, Dowzicky MJ. Regional variations in multidrug resistance among Enterobacteriaceae in the USA and comparative activity of tigecycline, a new glycylcycline antimicrobial. Int J Antimicrob Agents. May 2007;29(5):518-27. [Medline].

  21. Bush K, Jacoby GA, Medeiros AA. A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrob Agents Chemother. Jun 1995;39(6):1211-33. [Medline].

  22. Woodford N, Dallow JW, Hill RL, et al. Ertapenem resistance among Klebsiella and Enterobacter submitted in the UK to a reference laboratory. Int J Antimicrob Agents. Apr 2007;29(4):456-9. [Medline].

  23. Souli M, Kontopidou FV, Papadomichelakis E, et al. Clinical experience of serious infections caused by Enterobacteriaceae producing VIM-1 metallo-beta-lactamase in a Greek University Hospital. Clin Infect Dis. Mar 15 2008;46(6):847-54. [Medline].

  24. Pintado V, San Miguel LG, Grill F, et al. Intravenous colistin sulphomethate sodium for therapy of infections due to multidrug-resistant gram-negative bacteria. J Infect. Mar 2008;56(3):185-90. [Medline].

  25. Lo-Ten-Foe JR, de Smet AM, Diederen BM, et al. Comparative evaluation of the VITEK 2, disk diffusion, etest, broth microdilution, and agar dilution susceptibility testing methods for colistin in clinical isolates, including heteroresistant Enterobacter cloacae and Acinetobacter baumannii strains. Antimicrob Agents Chemother. Oct 2007;51(10):3726-30. [Medline].

  26. Gales AC, Jones RN, Sader HS. Global assessment of the antimicrobial activity of polymyxin B against 54 731 clinical isolates of Gram-negative bacilli: report from the SENTRY antimicrobial surveillance programme (2001-2004). Clin Microbiol Infect. Apr 2006;12(4):315-21. [Medline].

  27. Bassetti M, Righi E, Fasce R, et al. Efficacy of ertapenem in the treatment of early ventilator-associated pneumonia caused by extended-spectrum beta-lactamase-producing organisms in an intensive care unit. J Antimicrob Chemother. Aug 2007;60(2):433-5. [Medline].

  28. Abbott SL, Janda JM. Enterobacter cancerogenus ("Enterobacter taylorae") infections associated with severe trauma or crush injuries. Am J Clin Pathol. Mar 1997;107(3):359-61. [Medline].

  29. Alhambra A, Cuadros JA, Cacho J, et al. In vitro susceptibility of recent antibiotic-resistant urinary pathogens to ertapenem and 12 other antibiotics. J Antimicrob Chemother. Jun 2004;53(6):1090-4. [Medline].

  30. Caplan ES, Hoyt NJ. Identification and treatment of infections in multiply traumatized patients. Am J Med. Jul 15 1985;79(1A):68-76. [Medline].

  31. Clark NM, Patterson J, Lynch JP 3rd. Antimicrobial resistance among gram-negative organisms in the intensive care unit. Curr Opin Crit Care. Oct 2003;9(5):413-23. [Medline].

  32. Cosgrove SE, Kaye KS, Eliopoulous GM, et al. Health and economic outcomes of the emergence of third-generation cephalosporin resistance in Enterobacter species. Arch Intern Med. Jan 28 2002;162(2):185-90. [Medline].

  33. Cunha BA. Enterobacter: Colonization & infection. Infect Dis Pract. 1999;23:41-3.

  34. Cunha BA, Theodoris AC, Yannelli B. Enterobacter cloacae graft infection/bacteremia in a hemodialysis patient. Am J Infect Control. Apr 2000;28(2):181-3. [Medline].

  35. De Champs C, Sirot D, Chanal C, et al. A 1998 survey of extended-spectrum beta-lactamases in Enterobacteriaceae in France. The French Study Group. Antimicrob Agents Chemother. Nov 2000;44(11):3177-9. [Medline].

  36. Donati L, Scamazzo F, Gervasoni M, et al. Infection and antibiotic therapy in 4000 burned patients treated in Milan, Italy, between 1976 and 1988. Burns. Aug 1993;19(4):345-8. [Medline].

  37. Foster DR, Rhoney DH. Enterobacter meningitis: organism susceptibilities, antimicrobial therapy and related outcomes. Surg Neurol. Jun 2005;63(6):533-7; discussion 537. [Medline].

  38. Fritsche TR, Stilwell MG, Jones RN. Antimicrobial activity of doripenem (S-4661): a global surveillance report (2003). Clin Microbiol Infect. Dec 2005;11(12):974-84. [Medline].

  39. Fritsche TR, Strabala PA, Sader HS, et al. Activity of tigecycline tested against a global collection of Enterobacteriaceae, including tetracycline-resistant isolates. Diagn Microbiol Infect Dis. Jul 2005;52(3):209-13. [Medline].

  40. Gallagher PG. Enterobacter bacteremia in pediatric patients. Rev Infect Dis. Sep-Oct 1990;12(5):808-12. [Medline].

  41. Hanna H, Afif C, Alakech B, Boktour M, et al. Central venous catheter-related bacteremia due to gram-negative bacilli: significance of catheter removal in preventing relapse. Infect Control Hosp Epidemiol. Aug 2004;25(8):646-9. [Medline].

  42. Hoffmann H, Sturenburg E, Heesemann J, et al. Prevalence of extended-spectrum beta-lactamases in isolates of the Enterobacter cloacae complex from German hospitals. Clin Microbiol Infect. Apr 2006;12(4):322-30. [Medline].

  43. Jiang X, Ni Y, Jiang Y, et al. Outbreak of infection caused by Enterobacter cloacae producing the novel VEB-3 beta-lactamase in China. J Clin Microbiol. Feb 2005;43(2):826-31. [Medline].

  44. Kang CI, Kim SH, Park WB, et al. Bloodstream infections caused by Enterobacter species: predictors of 30-day mortality rate and impact of broad-spectrum cephalosporin resistance on outcome. Clin Infect Dis. Sep 15 2004;39(6):812-8. [Medline].

  45. Kaye KS, Cosgrove S, Harris A, et al. Risk factors for emergence of resistance to broad-spectrum cephalosporins among Enterobacter spp. Antimicrob Agents Chemother. Sep 2001;45(9):2628-30. [Medline].

  46. Larson EL, Cimiotti JP, Haas J, et al. Gram-negative bacilli associated with catheter-associated and non-catheter-associated bloodstream infections and hand carriage by healthcare workers in neonatal intensive care units. Pediatr Crit Care Med. Jul 2005;6(4):457-61. [Medline].

  47. Leverstein-van Hall MA, Blok HE, et al. Extensive hospital-wide spread of a multidrug-resistant enterobacter cloacae clone, with late detection due to a variable antibiogram and frequent patient transfer. J Clin Microbiol. Feb 2006;44(2):518-24. [Medline].

  48. Liu CP, Wang NY, Lee CM, et al. Nosocomial and community-acquired Enterobacter cloacae bloodstream infection: risk factors for and prevalence of SHV-12 in multiresistant isolates in a medical centre. J Hosp Infect. Sep 2004;58(1):63-77. [Medline].

  49. Livermore DM. beta-Lactamases in laboratory and clinical resistance. Clin Microbiol Rev. Oct 1995;8(4):557-84. [Medline].

  50. Livermore DM, Oakton KJ, Carter MW, et al. Activity of ertapenem (MK-0826) versus Enterobacteriaceae with potent beta-lactamases. Antimicrob Agents Chemother. Oct 2001;45(10):2831-7. [Medline].

  51. Luzzaro F, Docquier JD, Colinon C, et al. Emergence in Klebsiella pneumoniae and Enterobacter cloacae clinical isolates of the VIM-4 metallo-beta-lactamase encoded by a conjugative plasmid. Antimicrob Agents Chemother. Feb 2004;48(2):648-50. [Medline].

  52. Markowitz SM, Smith SM, Williams DS. Retrospective analysis of plasmid patterns in a study of burn unit outbreaks of infection due to Enterobacter cloacae. J Infect Dis. Jul 1983;148(1):18-23. [Medline].

  53. Mushtaq S, Ge Y, Livermore DM. Comparative activities of doripenem versus isolates, mutants, and transconjugants of Enterobacteriaceae and Acinetobacter spp. with characterized beta-lactamases. Antimicrob Agents Chemother. Apr 2004;48(4):1313-9. [Medline].

  54. Paterson DL, Rossi F, Baquero F, et al. In vitro susceptibilities of aerobic and facultative Gram-negative bacilli isolated from patients with intra-abdominal infections worldwide: the 2003 Study for Monitoring Antimicrobial Resistance Trends (SMART). J Antimicrob Chemother. Jun 2005;55(6):965-73. [Medline].

  55. Pitout JD, Nordmann P, Laupland KB, et al. Emergence of Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs) in the community. J Antimicrob Chemother. Jul 2005;56(1):52-9. [Medline].

  56. Pitout JD, Thomson KS, Hanson ND, et al. Plasmid-mediated resistance to expanded-spectrum cephalosporins among Enterobacter aerogenes strains. Antimicrob Agents Chemother. Mar 1998;42(3):596-600. [Medline].

  57. Ristuccia PA, Cunha BA. Enterobacter. Infect Control. Mar 1985;6(3):124-8. [Medline].

  58. Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs. 2003;63(4):353-65. [Medline].

  59. Sader HS, Jones RN, Dowzicky MJ, et al. Antimicrobial activity of tigecycline tested against nosocomial bacterial pathogens from patients hospitalized in the intensive care unit. Diagn Microbiol Infect Dis. Jul 2005;52(3):203-8. [Medline].

  60. Sader HS, Jones RN, Stilwell MG, et al. Tigecycline activity tested against 26,474 bloodstream infection isolates: a collection from 6 continents. Diagn Microbiol Infect Dis. Jul 2005;52(3):181-6. [Medline].

  61. Sanders CC, Sanders WE Jr. beta-Lactam resistance in gram-negative bacteria: global trends and clinical impact. Clin Infect Dis. Nov 1992;15(5):824-39. [Medline].

  62. Sanders WE Jr, Sanders CC. Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin Microbiol Rev. Apr 1997;10(2):220-41. [Medline].

  63. Siegel JD, Rhinehart E, Jackson M, Chiarello L and the HICPAC. Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Healthcare SEttings 2007. Centers for Disease Contol. Available at http://www.cdc.gov/ncidod/dhqp/pdf/guidelines/Isolation2007.pdf. Accessed 1 April 12008.

  64. Siegel JD, Rhinehart E, Jackson M, Chiarello L, HICPAC. Management of Multidrug-Resistant Organisms In Healthcare Settings, 2006. Centers for Disease Control. Available at http://www.cdc.gov/ncidod/dhqp/pdf/ar/mdroGuideline2006.pdf. accessed 1 April 2008.

  65. Tresoldi AT, Padoveze MC, Trabasso P, et al. Enterobacter cloacae sepsis outbreak in a newborn unit caused by contaminated total parenteral nutrition solution. Am J Infect Control. Jun 2000;28(3):258-61. [Medline].

  66. v Dijk Y, Bik EM, Hochstenbach-Vernooij S, v d Vlist GJ, Savelkoul PH, Kaan JA, et al. Management of an outbreak of Enterobacter cloacae in a neonatal unit using simple preventive measures. J Hosp Infect. May 2002;51(1):21-6. [Medline].

  67. Watson JT, Jones RC, Siston AM, et al. Outbreak of catheter-associated Klebsiella oxytoca and Enterobacter cloacae bloodstream infections in an oncology chemotherapy center. Arch Intern Med. Dec 12-26 2005;165(22):2639-43. [Medline].

  68. Wendt C, Lin D, von Baum H. Risk factors for colonization with third-generation cephalosporin-resistant enterobacteriaceae. Infection. Oct 2005;33(5-6):327-32. [Medline].

  69. Wisplinghoff H, Bischoff T, Tallent SM, et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis. Aug 1 2004;39(3):309-17. [Medline].

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Further Reading

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Keywords

Enterobacter infections, Enterobacter cloacae infection, Enterobacter aerogenes infection, Enterobacter sakazakii infection, Enterobacteriaceae infections, E cloacae, E aerogenes, E sakazakii, Enterobacter bacteremia, Enterobacter lower respiratory tract infection, Enterobacter skin infection, Enterobacter soft-tissue infection, Enterobacter urinary tract infection, Enterobacter UTI, Enterobacter endocarditis, Enterobacter intra-abdominal infection, Enterobacter intraabdominal infection, Enterobacter septic arthritis, Enterobacter osteomyelitis, Enterobacter ophthalmic infections, nosocomial Enterobacter infection, Enterobacter pneumonia, Enterobacter taylorae, E taylorae, Enterobacter cancerogenus, E cancerogenus

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Contributor Information and Disclosures

Author

Susan L Fraser, MD, Infectious Diseases Service, Walter Reed Army Medical Center; Chairman, Infection Control Committee; Associate Professor of Medicine, Uniformed Services University of the Health Sciences
Susan L Fraser, MD is a member of the following medical societies: American College of Physicians, American Liver Foundation, American Society for Microbiology, American Society of Tropical Medicine and Hygiene, Armed Forces Infectious Diseases Society, and Infectious Diseases Society of America
Disclosure: Nothing to disclose.

Coauthor(s)

Michael Arnett, MD, Resident, Department of Medicine, Tripler Army Medical Center
Disclosure: Nothing to disclose.

Christian P Sinave, MD, Associate Professor, Department of Medical Microbiology and Infectious Diseases, University of Sherbrooke, Canada
Christian P Sinave, MD is a member of the following medical societies: American Society for Microbiology and Canadian Infectious Disease Society
Disclosure: Nothing to disclose.

Medical Editor

Maria D Mileno, MD, Assistant Professor, Department of Internal Medicine, Division of Infectious Diseases, Brown University
Maria D Mileno, MD is a member of the following medical societies: Alpha Omega Alpha, American College of Physicians, American Society of Tropical Medicine and Hygiene, Infectious Diseases Society of America, International Society of Travel Medicine, and Sigma Xi
Disclosure: Nothing to disclose.

Pharmacy Editor

Francisco Talavera, PharmD, PhD, Senior Pharmacy Editor, eMedicine
Disclosure: Nothing to disclose.

Managing Editor

Joseph F John Jr, MD, FACP, FIDSA, FSHEA, Clinical Professor of Medicine, Molecular Genetics and Microbiology, Medical University of South Carolina; Associate Chief of Staff for Education, Ralph H Johnson Veterans Affairs Medical Center
Disclosure: BioMerieux Honoraria Review panel membership; Cubist Honoraria Review panel membership; Pfizer Honoraria Speaking and teaching; Merck Stock dividends stock holdings

CME Editor

Eleftherios Mylonakis, MD, Clinical and Research Fellow, Department of Internal Medicine, Division of Infectious Diseases, Massachusetts General Hospital
Eleftherios Mylonakis, MD is a member of the following medical societies: American Association for the Advancement of Science, American College of Physicians, American Society for Microbiology, and Infectious Diseases Society of America
Disclosure: Nothing to disclose.

Chief Editor

Burke A Cunha, MD, Professor of Medicine, State University of New York School of Medicine at Stony Brook; Chief, Infectious Disease Division, Winthrop-University Hospital
Burke A Cunha, MD is a member of the following medical societies: American College of Chest Physicians, American College of Physicians, and Infectious Diseases Society of America
Disclosure: Nothing to disclose.

 
 
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